Factors driving the assembly of prokaryotic communities in bulk soil and rhizosphere of Torreya grandis along a 900-year age gradient

Excessive nutrient inputs imperil the stability of forest ecosystems via modifying the interactions among soil properties, microbes, and plants, particularly in forests composed of cash crops that are under intensive disturbances of agricultural activities, such as Torreya grandis. Understanding the potential drivers of soil microbial community helps scientists develop effective strategies for balancing the protection and productivity of the ancient Torreya forest. Here, we assayed the link between plant and soil parameters and prokaryote communities in bulk soil and T. grandis rhizosphere in 900-year-old stands by detecting plant and soil properties in two independent sites in southeastern China. Our results showed no apparent influence of stand age on the compositions of prokaryote communities in bulk soil and T. grandis rhizosphere. In contrast, soil abiotic factors (i.e., soil pH) overwhelm plant characteristics (i.e., height, plant tissue carbon, nitrogen, and phosphorus content) and contribute most to the shift in prokaryote communities in bulk soil and T. grandis rhizosphere. Soil pH leads to an increase in microbiota alpha diversity in both compartments. With the help of a random forest, we found a critical transition point of pH (pH = 4.9) for the dominance of acidic and near-neutral bacterial groups. Co-occurrence network analysis further revealed a substantially simplified network in plots with a pH of <4.9 versus samples with a pH of ≥4.9, indicating that soil acidification induces biodiversity loss and disrupts potential interactions among soil microbes. Our findings provide empirical evidence that soil abiotic properties nearly completely offset the roles of host plants in the assembly and potential interactions of rhizosphere microorganisms. Hence, reduction in inorganic fertilization and proper liming protocols should be seriously considered by local farmers to protect ancient Torreya forests.